Role of thioredoxin-1 in ischemic preconditioning, postconditioning and aged ischemic hearts

Pharmacological Research

Volumn 109, Issue , 2016, Pages 24-31

  D'Annunzio, Veronica ^a,b   Perez, Virginia ^a,b   Boveris, Alberto ^a   Gelpi, Ricardo J ^a,b   Poderoso, Juan J ^b  

^a University of Buenos Aires   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Aging; Heart; Ischemia reperfusion; Postconditioning; Preconditioning; Thioredoxin

Indexed keywords

GLUTATHIONE; GLUTATHIONE DISULFIDE; GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE 2; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; REACTIVE OXYGEN METABOLITE; RESVERATROL; THIOREDOXIN 1; THIOREDOXIN 2; THIOREDOXIN;

AGING; APOPTOSIS; ARTICLE; CELL SURVIVAL; CORONARY ARTERY OCCLUSION; ENDOTHELIUM CELL; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEART PROTECTION; HUMAN; ISCHEMIC HEART DISEASE; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; ANIMAL; CARDIAC MUSCLE; CORONARY BLOOD VESSEL; HEART; METABOLISM; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; PATHOPHYSIOLOGY; PHYSIOLOGY;

AGING; ANIMALS; CORONARY VESSELS; HEART; HUMANS; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; THIOREDOXINS;

EID: 84961793442     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2016.03.009     Document Type: Article

References (96)

1. T. Ago, and J. Sadoshima Thioredoxin and ventricular remodeling J. Mol. Cell Cardiol. 41 2006 762 773
2. H. Nakamura, Y. Hoshino, Y. Okuyama, and J. Yodoi Thioredoxin 1 as a new therapeutics Adv. Drug Rev. 61 4 2009 303 309
3. T.C. Laurent, E.C. Moore, and P. Reichard Enzymatic synthesis of deoxyribonucleotides IV. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B J. Biol. Chem. 239 1964 3436 3444
4. A. Holmgren, B.O. Söderberg, H. Eklund, and C.I. Brändén Three-dimensional structure of Escherichia coli thioredoxin-S2 to 28 Å resolution U. S. A. Proc. Natl. Acad. Sci. 72 6 1975 2305 2309
5. Jean-Francois Collet and Joris messens structure, function, and mechanism of thioredoxin proteins Antioxid. Redox Signal. 13 2010 1205 1216
6. K. Shioji, C. Kishimoto, H. Nakamura, H. Masutani, Z. Yuan, S. Oka, and J. Yodoi Overexpression of thioredoxin-1 in transgenic mice attenuates adriamycin-induced cardiotoxicity Circulation 106 11 2002 1403 1409
7. T. Rassaf, and P. Luedike Between nitros(yl) ation and nitration: regulation of thioredoxin-1 in myocardial ischemia/reperfusion injury J. Mol. Cell Cardiol. 49 3 2010 343 346
8. T. Turoczi, V.W. Chang, R.M. Engelman, N. Maulik, Y.S. Ho, and D.K. Das Thioredoxin redox signaling in the ischemic heart: an insight with transgenic mice overexpressing Trx1 J. Mol. Cell Cardiol. 35 6 2003 695 704
9. S. Matsushima, D. Zablocki, and J. Sadoshima Application of recombinant thioredoxin1 for treatment of heart desease J. Mol. Cell Cardiol. 51 4 2011 570 573
10. A. Mitsui, J. Hamuro, H. Nakamura, N. Kondo, Y. Hirabayashi, S. Ishizaki-Koizumi, T. Hirakawa, T. Inoue, and J. Yodoi Overexpression of human thioredoxin in transgenic mice controls oxidative stress and life span Antioxid. Redox Signal. 4 2002 693 696
11. S. Kaga, L. Zhan, M. Matsumoto, and N. Maulik Resveratrol enhances neovascularization in the infarcted rat myocardium through the induction of thioredoxin-1: heme oxygenase-1 and vascular endothelial growth factor J. Mol. Cell Cardiol. 39 5 2005 813 822
12. J. Altschmied, and J. Haendeler Thioredoxin-1 and endothelial cell aging: role in cardiovascular diseases Antioxid. Redox Signal. 11 2009 1733 1740
13. M. Aota, K. Matsuda, N. Isowa, H. Wada, J. Yodoi, and T. Ban Protection against reperfusion-induced arrhythmias by human thioredoxin J. Cardiovasc. Pharmacol. 27 5 1996 727 732
14. H. Nakamura, J. Vaage, G. Valen, C.A. Padilla, M. Björnstedt, and A. Holmgren Measurements of plasma glutaredoxin and thioredoxin in healthy volunteers and during open-heart surgery Free Radic. Biol. Med. 24 7-8 1998 1176 1186
15. M. Kihlström Protection effect of endurance training against reoxygenation-induced injuries in rat heart J. Appl. Physiol. 68 4 1990 1672 1678
16. L. Tao, E. Gao, N.S. Bryan, Y. Qu, H.R. Liu, A. Hu, T.A. Christopher, B.L. Lopez, J. Yodoi, W.J. Koch, M. Feelisch, and X.L. Ma Cardioprotective effects of thioredoxin in myocardial ischemia and reperfusion: role of S-nitrosation Proc. Natl. Acad. Sci. U. S. A. 101 31 2004 11471 11476
17. E.J. Meuillet, D. Mahadevan, M. Berggren, A. Coon, and G. Powis Thioredoxin-1 binds to the C2 domain of PTEN inhibiting PTEN's lipid phosphatase activity and membrane binding: a mechanism for the functional loss of PTEN's tumor suppressor activity Arch. Biochem. Biophys. 429 2 2004 123 133
18. M.K. Saini, and S.N. Sanyal PTEN regulates apoptotic cell death through PI3-K/Akt/GSK3β signaling pathway in DMH induced early colon carcinogenesis in rat Exp. Mol. Pathol. 93 1 2012 135 146
19. H.L. Ha, and D.Y. Yu HBx-induced reactive oxygen species activates hepatocellular carcinogenesis via dysregulation of PTEN/Akt pathway World J. Gastroenterol. 16 39 2010 4932 4937
20. L. Zu, X. Zheng, B. Wang, N. Parajuli, C. Steenbergen, L.C. Becker, and Z.P. Cai Ischemic preconditioning attenuates mitochondrial localization of PTEN induced by ischemia-reperfusion Am. J. Physiol. Heart Circ. Physiol. 300 6 2011 2177 2186
21. D.M. Flaherty, M.M. Monick, and S.L. Hinde Human alveolar macrophages are deficient in PTEN J. Biol. Chem. 281 8 2006 5058 5064
22. D.J. Hausenloy, and D.M. Yellon Reperfusion injury salvage kinase signalling: taking a RISK for cardioprotection Heart Fail. Rev. 12 3-4 2007 217 234
23. C. Penna, M.G. Perrelli, and P. Pagliaro Mitochondrial pathways, permeability transition pore, and redox signaling in cardioprotection: therapeutic implications Antioxid. Redox Signal. 18 5 2013 556 599
24. S. Sanada, I. Komuro, and M. Kitakaze Pathophysiology of myocardial reperfusion injury: preconditioning, postconditioning, and translational aspects of protective measures Am. J. Physiol. Heart Circ. Physiol. 301 5 2011 H1723 H1741
25. H. Ge, M. Zhao, S. Lee, and Z. Xu Mitochondrial Src tyrosine kinase plays a role in the cardioprotective effect of ischemic preconditioning by modulating complex I activity and mitochondrial ROS generation Free Radic. Res. 49 10 2015 1210 1217
26. P. Yu, J. Zhang, S. Yu, Z. Luo, F. Hua, L. Yuan, Z. Zhou, Q. Liu, X. Du, S. Chen, L. Zhang, and G. Xu Protective effect of sevoflurane postconditioning against cardiac Ischemia/Reperfusion injury via ameliorating mitochondrial impairment oxidative stress and rescuing autophagic clearance PLoS One 10 8 2015 e0134666
27. C.E. Murry, R. Jennings, and K.A. Reimer Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium Circulation 74 1986 1124 1136
28. A. Cave, G. Horowitz, and C. Apstein Can ischemic preconditioning protect against hypoxia-induced damage? Studies of contractile function in isolated rat hearts J. Mol. Cell Cardiol. 26 1994 1471 1486
29. K. Ytrehus, Y. Liu, and J. Downey Preconditioning protects ischemic rabbit heart by protein kinase C activation Am. J. Physiol. 266 1994 H1145 H1152
30. G.S. Liu, J. Thornton, D.M. Van Winkle, A.W. Stanley, R.A. Olsson, and J.M. Downey Protection against infarction afforded by preconditioning is mediated by A1 adenosine receptors in rabbit heart Circulation 84 1991 350 356
31. M. Leesar, M. Stoddard, M. Ahmed, J. Broadbent, and R. Bolli Preconditioning of human miocardium with adenosine during coronary angioplasty Circulation 95 1997 2500 2507
32. V.J. McIntosh, and R.D. Lasley Adenosine receptor-mediated cardioprotection: are all 4 subtypes required or redundant? J. Cardiovasc. Pharmacol. Ther. 17 1 2012 21 33
33. A. Banerjee, C. Locke-Winter, K.B. Rogers, M.B. Mitchell, E.C. Brew, C.B. Cairns, D.D. Bensard, and A.H. Harken Preconditioning against myocardial dysfunction after ischemia and reperfusion by an alpha 1-adrenergic mechanism Circ. Res. 73 1993 656 670
34. O. Oldenburg, Q. Qin, A.R. Sharma, M.V. Cohen, J.M. Downey, and J.N. Benoit Acetylcholine leads to free radical production dependent on K(ATP) channels, G(i) proteins, phosphatidylinositol 3-kinase and tyrosine kinase Cardiovasc. Res. 55 2002 544 552
35. T. Krieg, L. Cui, Q. Qin, M.V. Cohen, J.M. Downey, and R.O.S. Mitochondrial generation following acetylcholine-induced EGF receptor transactivation requires metalloproteinase cleavage of proHB-EGF J. Mol. Cell Cardiol. 36 2004 435 443
36. C.S. Carr, R.J. Hill, H. Masamune, S.P. Kennedy, D.R. Knight, W.R. Tracey, and D.M. Yellon Evidence for a role for both the adenosine A1 and A3 receptors in protection of isolated human atrial muscle against simulated ischaemia Cardiovasc. Res. 36 1997 52 59
37. H. Takano, R. Bolli, R.G. Black Jr., E. Kodani, X.L. Tang, Z. Yang, S. Bhattacharya, and J.A. Auchampach A(1) or A(3) adenosine receptors induce late preconditioning against infarction in conscious rabbits by different mechanisms Circ. Res. 88 2001 520 528
38. M.V. Cohen, C.P. Baines, and J.M. Downey Ischemic preconditioning: from adenosine receptor to KATP channel Annu. Rev. Physiol. 10 2000 62 79
39. C. Page, and A.F. Doubell Mitogen-activated protein kinase (MAPK) in cardiac tissues Mol. Cell Biochem. 157 1996 12 26
40. Y. Wang Mitogen-activated protein kinases in heart development and diseases Circulation 116 2007 1413 1423
41. C.P. Baines, M.V. Cohen, and J.M. Downey Signal transduction in ischemic preconditioning: the role of kinases and mitochondrial K(ATP) channels J. Cardiovasc. Electrophysiol. 10 1999 741 754
42. N. Maulik, M. Watanabe, Y.L. Zu, C.K. Huang, G.A. Cordis, J.A. Schley, and D.K. Das Ischemic preconditioning triggers the activation of MAP kinases and MAPKAP kinase 2 in rat hearts FEBS Lett. 396 1996 233 237
43. N. Maulik, M. Sato, B.D. Price, and D.K. Das An essential role of NFkappaB in tyrosine kinase signaling of p38 MAP kinase regulation of myocardial adaptation to ischemia FEBS Lett. 429 3 1998 365 369
44. Z. Yao, J. Tong, X. Tan, C. Li, Z. Shao, W.C. Kim, T.L. vanden Hoek, L.B. Becker, C.A. Head, and P.T. Schumacker Role of reactive oxygen species in acetylcholine-induced preconditioning in cardiomyocytes Am. J. Physiol. 277 1999 H2504 2509
45. O. Oldenburg, S.D. Critz, M.V. Cohen, and J.M. Downey Acetylcholine-induced production of reactive oxygen species in adult rabbit ventricular myocytes is dependent on phosphatidylinositol 3- and Src-kinase activation and mitochondrial K (ATP) channel opening J. Mol. Cell Cardiol. 35 2003 653 660
46. L.B. Valdez, T. Zaobornyj, S. Bombicino, D.E. Iglesias, A. Boveris, M. Donato, V. D'Annunzio, B. Buchholz, R.J. Gelpi, and I. Complex syndrome in myocardial stunning and the effect of adenosine Free Radic. Biol. Med. 51 6 2011 1203 1212
47. L.B. Becker New concepts in reactive oxygen species and cardiovascular reperfusion physiology Cardiovasc. Res. 15 3 2004 461 470
48. M.L. Hess, and R.C. Kukreja Free radicals, calcium homeostasis, heat shock proteins, and myocardial stunning Ann. Thorac. Surg. 60 3 1995 760 766
49. H. Nakamura, K. Nakamura, and J. Yodoi Redox regulation of cellular activation Annu. Rev. Immunol. 15 1997 351 369
50. C.C. Chiueh, T. Andoh, and P.B. Chock Induction of thioredoxin and mitochondrial survival proteins mediates preconditioning-induced cardioprotection and neuroprotection Ann. N. Y. Acad. Sci. 1042 2005 403 418
51. T. Ago, I. Yeh, M. Yamamoto, M. Schinke-Braun, J.A. Brown, B. Tian, and J. Sadoshima Thioredoxin1 upregulates mitochondrial proteins related to oxidative phosphorylation and TCA cycle in the heart Antioxid. Redox Signal. 8 9-10 2006 1635 1650
52. D.K. Das, and N. Maulik Preconditioning potentiates redox signaling and converts death signal into survival signal Arch. Biochem. Biophys. 420 2 2003 305 311
53. Z.Q. Zhao, J.S. Corvera, M.E. Halkos, F. Kerendi, N.P. Wang, R.A. Guyton, and J. Vinten-Johansen Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning Am. J. Physiol. Heart Circ. Physiol. 285 2003 H579 H588
54. A. Tsang, D.J. Hausenloy, M.M. Mocanu, and Yellon D.M. Postconditioning a form of modified reperfusion protects the myocardium by activating the phosphatidylinositol 3-kinase-Akt pathway Circ. Res. 95 2004 230 232
55. X.M. Yang, J.B. Proctor, L. Cui, T. Krieg, J.M. Downey, and M.V. Cohen Multiple, Brief coronary occlusions during early reperfusion protect rabbit hearts by targeting cell signaling pathways J. Am. Coll. Cardiol. 44 2004 1103 1110
56. G. Gritsopoulos, E.K. Iliodromitis, A. Zoga, D. Farmakis, E. Demerouti, A. Papalois, I.A. Paraskevaidis, and D.T. Kremastinos Remote postconditioning is more potent than classic postconditioning in reducing the infarct size in anesthetized rabbits Cardiovasc. Drugs Ther. 23 3 2009 193 198
57. D. Weihrauch, J.G. Krolikowski, M. Bienengraeber, J.R. Kersten, and D.C. Warltier Pagel Morphine enhances isoflurane-induced postconditioning against myocardial infarction: the role of phosphatidylinositol-3-kinase and opioid receptors in rabbits Anesth. Analg. 101 2005 942 949
58. H.Y. Sun, N.P. Wang, F. Kerendi, M. Halkos, H. Kin, R.A. Guyton, J. Vinten-Johansen, and Z.Q. Zhao Hypoxic postconditioning reduces cardiomyocyte loss by inhibiting ROS generation and intracellular Ca2+ overload Am. J. Physiol. Heart Circ. Physiol. 288 2005 H1900 H1908
59. C.E. Darling, P.B. Solari, C.S. Smith, M.I. Furman, and K. Przyklenk Postconditioning' the human heart: multiple balloon inflations during primary angioplasty may confer cardioprotection Basic Res. Cardiol. 102 2007 274 278
60. H. Kin, Z.Q. Zhao, H.Y. Sun, N.P. Wang, J.S. Corvera, M.E. Halkos, F. Kerendi, R.A. Guyton, and J. Vinten-Johansen Postconditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion Cardiovasc. Res. 62 2004 74 85
61. V. D'Annunzio, M. Donato, L. Erni, V. Miksztowicz, B. Buchholz, C.L. Carrión, L. Schreier, R. Wikinski, R.J. Gelpi, G. Berg, and N. Basso Rosuvastatin given during reperfusion decreases infarct size and inhibits matrix metalloproteinase-2 activity in normocholesterolemic and hypercholesterolemic rabbits J. Cardiovasc. Pharmacol. 53 2 2009 137 144
62. M. Donato, V. D'Annunzio, B. Buchholz, V. Miksztowicz, C.L. Carrión, L.B. Valdez, T. Zaobornyj, L. Schreier, R. Wikinski, A. Boveris, G. Berg, and R.J. Gelpi Role of matrix metalloproteinase-2 in the cardioprotective effect of ischaemic postconditioning Exp. Physiol. 95 2 2010 274 281
63. V. D'Annunzio, M. Donato, B. Buchholz, V. Pérez, V. Miksztowicz, G. Berg, and R.J. Gelpi High cholesterol diet effects on ischemia-reperfusion injury of the heart Can. J. Physiol. Pharmacol. 90 9 2012 1185 1196
64. B. Buchholz, V. Dánnunzio, J.F. Giani, N. Siachoque, F.P. Dominici, D. Turyn, V. Perez, M. Donato, and R.J. Gelpi Ischemic postconditioning reduces infarct size through the α1-Adrenergic receptor pathway J. Cardiovasc. Pharmacol. 63 2014 504 511
65. M. Donato, V. D'Annunzio, G. Berg, G. Gonzalez, L. Schreier, C. Morales, R.L. Wikinski, and R.J. Gelpi Ischemic postconditioning reduces infarct size by activation of A1 receptors and K+(ATP) channels in both normal and hypercholesterolemic rabbits J. Cardiovasc. Pharmacol. 49 5 2007 287 292
66. B. Buchholz, V. Perez, N. Siachoque, V. Miksztowicz, G. Berg, M. Rodríguez, M. Donato, and R.J. Gelpi Dystrophin proteolysis: a potential target for MMP-2 and its prevention by ischemic preconditioning Am. J. Physiol. Heart Circ. Physiol. 307 1 2014 H88 96
67. A. Skyschally, R. Schulz, and G. Heusch Pathophysiology of myocardial infarction: protection by ischemic pre- and postconditioning Herz 33 2 2008 88 100
68. V. Perez, V. Dánnunzio, T. Mazo, T. Marchini, L. Cáceres, P. Evelson, and R.J. Gelpi Ischemic postconditioning confers cardioprotection and prevents reduction of Trx-1 in young mice, but not in middle-aged and old mice Mol. Cell Biochem. 2016 10.1007/s11010-016-2677-2
69. B.J. Cusack, P.S. Mushlin, T. Andrejuk, L.D. Voulelis, and R.D. Olson Aging alters the force-frequency relationship and toxicity of oxidative stress in rabbit heart Life Sci. 48 1991 1769 1777
70. V.V. Frolkis, R.A. Frolkis, L.S. Mkhitarian, and V.E. Fraifeld Age-dependent effects of ischemia and reperfusion on cardiac function and Ca2+ transport in myocardium Gerontology 37 1991 233 239
71. E.J. Lesnefsky, D.S. Gallo, J. Ye, T.S. Whittingham, and W.D. Lust Aging increases ischemia-reperfusion injury in the isolated, buffer perfused heart J. Lab. Clin. Med. 124 1994 843 851
72. E.J. Lesnefsky, C.F. Lundergan, J.M. Hodgson, R. Nair, J.S. Reiner, S.W. Greenhouse, R.M. Califf, and A.M. Ross Increased left ventricular dysfunction in elderly patients despite successful thrombolysis: the GUSTO-I angiographic experience J. Am. Coll. Cardiol. 28 1996 331 337
73. W.D. Flitter Free radicals and myocardial reperfusion injury Br. Med. Bull. 49 1993 545 555
74. K. Atake, D. Chen, S. Levitsky, E. Jimenez, and H. Feinberg Effect of aging on intracellular Ca2+, pHi, and contractility during ischemia and reperfusion Circulation 86 1992 371 376
75. B. Van der Loo, R. Labugger, J.N. Skepper, M. Bachschmid, J. Kilo, J.M. Powell, M. Palacios-Callender, J.D. Etrusalimsky, T. Quashning, T. Malinski, D. Gygi, V. Ullrich, and T.F. Luscher Enhanced peroxynitrite formation is associated with vascular aging J. Exp. Med. 192 2000 1731 1744
76. K. Asai, R.K. Kudej, Y.T. Shen, G.P. Yang, G. Takagi, A.B. Kidej, Y.J. Geng, N. Sato, J.B. Nazareno, D.E. Vatner, F. Natividad, S.P. Bishop, and S.F. Vatner Peripheral vascular endothelial dysfunction and apoptosis in old monkeys Arterioscler. Thromb. Vasc. Biol. 20 2000 1493 1499
77. J. Hoffmann, J. Haendeler, A. Aicher, L. Rossig, M. Vasa, A.M. Zeiher, and S. Dimmeler Aging enhances the sensitivity of endothelial cells toward apoptotic stimuli: important role of nitric oxide Circ. Res. 89 2001 709 715
78. P. Liu, B. Xu, T.A. Cavalieri, and C.E. Hock Age-related difference in myocardial function and inflammation in a rat model of myocardial ischemia-reperfusion Cardiovasc. Res. 56 2002 443 453
79. P. Liu, B. Xu, T.A. Cavalieri, and C.E. Hock Attenuation of antioxidative capacity enhances reperfusion injury in aged rat myocardium after MI/R Am. J. Physiol. Heart Circ. Physiol. 287 2004 2719 2727
80. P. Ferdinandy, D.J. Hausenloy, G. Heusch, G.F. Baxter, and R. Schulz Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning Pharmacol. Rev. 66 4 2014 1142 1174
81. K. Przyklenk Efficacy of cardioprotective 'conditioning' strategies in aging and diabetic cohorts: theco-morbidity conundrum Drugs Aging 28 5 2011 331 343
82. K. Boengler, R. Schulz, and G. Heusch Loss of cardioprotection with ageing Cardiovasc. Res. 83 2 2009 247 261
83. P. Abete, C. Napoli, G. Santoro, N. Ferrara, I. Tritto, M. Chiariello, F. Renco, and G. Ambrosio Age-related decrease in cardiac tolerance to oxidative stress J. Mol. Cell Cardiol. 31 1999 227 236
84. R.A. Fenton, E.W. Dickson, T.E. Meyer, and J.G. Dobson Aging reduces the cardioprotective effect of ischemic preconditioning in the rat heart J. Mol. Cell Cardiol. 32 2000 1371 1375
85. M.S. Sumeray, and D.M. Yellon Characterisation and validation of a murine model of global ischaemiareperfusion injury Mol. Cell Biochem. 186 1998 61 68
86. L. Willems, A. Zatta, K. Holgren, K.J. Ashton, and J.P. Headrick Age-related changes in ischemic tolerance in male and female mouse hearts J. Mol. Cell Cardiol. 38 2 2005 245 256
87. H. Zhang, L. Tao, X. Jiao, E. Gao, B.L. Lopez, T.A. Christopher, W. Koch, and X.L. Ma Nitrative thioredoxin inactivation as a cause of enhanced myocardial ischemia/reperfusion injury in the aging heart Free Radic. Biol. Med. 43 2007 39 47
88. G. Azhar, W. Gao, L. Liu, and J.Y. Wei Ischemia-reperfusion in the adult mouse heart influence of age Exp. Gerontol. 34 1999 699 714
89. K. Boengler, I. Konietzka, A. Buechert, Y. Heinen, D. Garcia-Dorado, G. Heusch, and R. Schulz Loss of ischemic preconditioning's cardioprotection in aged mouse hearts is associated with reduced gap junctional and mitochondrial levels of connexin 43 Am. J. Physiol. Heart Circ. Physiol. 292 4 2007 H1764 9
90. G.S. Uhl, and P.W. Farrell Myocardial infarction in young adults: risk factors and natural history Am. Heart J. 105 1983 548 553
91. D. Cohen, D.G. Manuel, P. Tugwell, T. Ramsay, and C. Sanmartin Inequity in primary and secondary preventive care for acute myocardial infarction? Use by socioeconomic status across middle-aged and older patients Can. J. Cardiol. 29 2013 1579 1585
92. Q. Fan, M. Chen, X. Fang, W.B. Lau, L. Xue, L. Zhao, H. Zhang, Y.H. Liang, X. Bai, H.Y. Niu, J. Ye, Q. Chen, X. Yang, and M. Liu Aging might augment reactive oxygen species (ROS) formation and affect reactive nitrogen species (RNS) level after myocardial ischemia/reperfusion in both humans and rats Age (Dordr.) 35 2013 1017 1026
93. E. Babušíková, J. Lehotský, D. Dobrota, P. Račay, and P. Kaplán Age-associated changes in Ca(2+)-ATPase and oxidative damage in sarcoplasmic reticulum of rat heart Physiol. Res. 61 2012 453 460
94. K.B. Choksi, J.E. Nuss, J.H. DeFord, and J. Papaconstantinou Mitochondrial electron transport chain functions in longlived Ames dwarf mice Aging (Milano) 3 8 2011 754 767
95. J.Y. Kim, O.Y. Kim, J.K. Paik, D.Y. Kwon, H.J. Kim, and J.H. Lee Association of age-related changes in circulating intermediary lipid metabolites, inflammatory and oxidative stress markers, and arterial stiffness in middle-aged men Age (Dordr.) 35 2013 1507 1519
96. V. Dánnunzio, V. Perez, T. Mazo, B. Buchholz, M.C. Carreras, J.J. Poderoso, J. Sadoshima, and R.J. Gelpi Loss of myocardial protection against myocardial infarction in middle aged transgenic mice overexpressing cardiac thioredoxin-1 Oncotarget 2016 10.18632/oncotarget.7726